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Genetic relatedness of multidrug resistant Escherichia coli isolated from humans, chickens and poultry environments

BACKGROUND: Inappropriate use of antimicrobial agents in animal production has led to the development of antimicrobial resistance (AMR) in foodborne pathogens. Transmission of AMR foodborne pathogens from reservoirs, particularly chickens to the human population does occur. Recently, we reported tha...

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Autores principales: Aworh, Mabel Kamweli, Kwaga, Jacob K. P., Hendriksen, Rene S., Okolocha, Emmanuel C., Thakur, Siddhartha
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7988975/
https://www.ncbi.nlm.nih.gov/pubmed/33757589
http://dx.doi.org/10.1186/s13756-021-00930-x
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author Aworh, Mabel Kamweli
Kwaga, Jacob K. P.
Hendriksen, Rene S.
Okolocha, Emmanuel C.
Thakur, Siddhartha
author_facet Aworh, Mabel Kamweli
Kwaga, Jacob K. P.
Hendriksen, Rene S.
Okolocha, Emmanuel C.
Thakur, Siddhartha
author_sort Aworh, Mabel Kamweli
collection PubMed
description BACKGROUND: Inappropriate use of antimicrobial agents in animal production has led to the development of antimicrobial resistance (AMR) in foodborne pathogens. Transmission of AMR foodborne pathogens from reservoirs, particularly chickens to the human population does occur. Recently, we reported that occupational exposure was a risk factor for multidrug-resistant (MDR) Escherichia coli (E. coli) among poultry-workers. Here we determined the prevalence and genetic relatedness among MDR E. coli isolated from poultry-workers, chickens, and poultry environments in Abuja, Nigeria. This study was conducted to address the gaps identified by the Nigerian AMR situation analysis. METHODS: We conducted a cross-sectional study among poultry-workers, chickens, and poultry farm/live bird market (LBM) environments. The isolates were tested phenotypically for their antimicrobial susceptibility profiles, genotypically characterized using whole-genome sequencing (WGS) and in silico multilocus sequence types (MLST). We conducted a phylogenetic single nucleotide polymorphism (SNPs) analysis to determine relatedness and clonality among the isolates. RESULTS: A total of 115 (26.8%) out of 429 samples were positive for E. coli. Of these, 110 isolates were viable for phenotypic and genotypic characterization. The selection comprised 47 (42.7%) isolates from poultry-workers, 36 (32.7%) from chickens, and 27 (24.5%) from poultry-farm or LBM environments. Overall, 101 (91.8%) of the isolates were MDR conferring resistance to at least three drug classes. High frequency of resistance was observed for tetracycline (n = 102; 92.7%), trimethoprim/sulfamethoxazole (n = 93; 84.5%), streptomycin (n = 87; 79.1%) and ampicillin (n = 88; 80%). Two plasmid-mediated colistin genes—mcr-1.1 harboured on IncX4 plasmids were detected in environmental isolates. The most prevalent sequence types (ST) were ST-155 (n = 8), ST-48 (n = 8) and ST-10 (n = 6). Two isolates of human and environmental sources with a SNPs difference of 6161 originating from the same farm shared a novel ST. The isolates had similar AMR genes and plasmid replicons. CONCLUSION: MDR E.coli isolates were prevalent amongst poultry-workers, poultry, and the poultry farm/LBM environment. The emergence of MDR E. coli with novel ST in two isolates may be plasmid-mediated. Competent authorities should enforce AMR regulations to ensure prudent use of antimicrobials to limit the risk of transmission along the food chain. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s13756-021-00930-x.
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spelling pubmed-79889752021-03-25 Genetic relatedness of multidrug resistant Escherichia coli isolated from humans, chickens and poultry environments Aworh, Mabel Kamweli Kwaga, Jacob K. P. Hendriksen, Rene S. Okolocha, Emmanuel C. Thakur, Siddhartha Antimicrob Resist Infect Control Research BACKGROUND: Inappropriate use of antimicrobial agents in animal production has led to the development of antimicrobial resistance (AMR) in foodborne pathogens. Transmission of AMR foodborne pathogens from reservoirs, particularly chickens to the human population does occur. Recently, we reported that occupational exposure was a risk factor for multidrug-resistant (MDR) Escherichia coli (E. coli) among poultry-workers. Here we determined the prevalence and genetic relatedness among MDR E. coli isolated from poultry-workers, chickens, and poultry environments in Abuja, Nigeria. This study was conducted to address the gaps identified by the Nigerian AMR situation analysis. METHODS: We conducted a cross-sectional study among poultry-workers, chickens, and poultry farm/live bird market (LBM) environments. The isolates were tested phenotypically for their antimicrobial susceptibility profiles, genotypically characterized using whole-genome sequencing (WGS) and in silico multilocus sequence types (MLST). We conducted a phylogenetic single nucleotide polymorphism (SNPs) analysis to determine relatedness and clonality among the isolates. RESULTS: A total of 115 (26.8%) out of 429 samples were positive for E. coli. Of these, 110 isolates were viable for phenotypic and genotypic characterization. The selection comprised 47 (42.7%) isolates from poultry-workers, 36 (32.7%) from chickens, and 27 (24.5%) from poultry-farm or LBM environments. Overall, 101 (91.8%) of the isolates were MDR conferring resistance to at least three drug classes. High frequency of resistance was observed for tetracycline (n = 102; 92.7%), trimethoprim/sulfamethoxazole (n = 93; 84.5%), streptomycin (n = 87; 79.1%) and ampicillin (n = 88; 80%). Two plasmid-mediated colistin genes—mcr-1.1 harboured on IncX4 plasmids were detected in environmental isolates. The most prevalent sequence types (ST) were ST-155 (n = 8), ST-48 (n = 8) and ST-10 (n = 6). Two isolates of human and environmental sources with a SNPs difference of 6161 originating from the same farm shared a novel ST. The isolates had similar AMR genes and plasmid replicons. CONCLUSION: MDR E.coli isolates were prevalent amongst poultry-workers, poultry, and the poultry farm/LBM environment. The emergence of MDR E. coli with novel ST in two isolates may be plasmid-mediated. Competent authorities should enforce AMR regulations to ensure prudent use of antimicrobials to limit the risk of transmission along the food chain. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s13756-021-00930-x. BioMed Central 2021-03-23 /pmc/articles/PMC7988975/ /pubmed/33757589 http://dx.doi.org/10.1186/s13756-021-00930-x Text en © The Author(s) 2021 Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data.
spellingShingle Research
Aworh, Mabel Kamweli
Kwaga, Jacob K. P.
Hendriksen, Rene S.
Okolocha, Emmanuel C.
Thakur, Siddhartha
Genetic relatedness of multidrug resistant Escherichia coli isolated from humans, chickens and poultry environments
title Genetic relatedness of multidrug resistant Escherichia coli isolated from humans, chickens and poultry environments
title_full Genetic relatedness of multidrug resistant Escherichia coli isolated from humans, chickens and poultry environments
title_fullStr Genetic relatedness of multidrug resistant Escherichia coli isolated from humans, chickens and poultry environments
title_full_unstemmed Genetic relatedness of multidrug resistant Escherichia coli isolated from humans, chickens and poultry environments
title_short Genetic relatedness of multidrug resistant Escherichia coli isolated from humans, chickens and poultry environments
title_sort genetic relatedness of multidrug resistant escherichia coli isolated from humans, chickens and poultry environments
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7988975/
https://www.ncbi.nlm.nih.gov/pubmed/33757589
http://dx.doi.org/10.1186/s13756-021-00930-x
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